Differential deployment of sanctioning mechanisms by male and female host trees in a gynodioecious fig–wasp mutualism

Abstract

In some insect nursery pollination mutualisms, plant hosts impose net costs to uncooperative “cheater” symbionts. These “sanctions” promote mutualism stability but their precise adaptive nature remains unclear. In fig–wasp mutualisms host trees (Ficus spp.) are only pollinated by female agaonid wasps whose larvae only use galled fig flowers as food. In actively pollinated systems, if wasps fail to pollinate, sanctions can result via fig abortion, killing all wasp offspring, or by increased offspring mortality within un‐aborted figs. These sanctions result from selective investment to pollinated inflorescences, a mechanism present in almost all angiosperms. To more fully understand how selective investment functions as sanctions requires the measurement of variation in their costs and benefits to both hosts and symbionts. Gynodioecious fig‐tree–fig‐wasp mutualisms are particularly suitable for this because pollen and wasps are produced only in the figs of “male” trees and seeds only in the figs of “female” trees. Male and female trees thus incur different net costs of pollen absence, and costs of sanctions to pollen‐free “cheater” wasps only occur in male trees. We used the actively pollinated host tree Ficus hispida and introduced into male and female figs either 1, 3, 5, 7, or 9 all pollen‐laden “cooperative” (P+) or all pollen‐free “cheater” (P−) wasps. Abortion in both male and female trees was highest in P− figs, with P− fig abortion higher in females (~90%) than in males (~40%). Fig abortion was negatively associated with foundress number mainly in P+ figs; in P− figs abortion was only weakly associated with the number of “cheater” wasps, especially in female figs. In un‐aborted male figs, wasp offspring mortality was higher in P− figs than in P+ figs, and in P− figs correlated positively with foundress (cheater) number. Increased offspring mortality was biased against female wasp offspring and likely resulted from reduced larval nutrition in unpollinated flowers. Variation in selective investment to P− figs thus reflects costs and benefits of pollen absence/presence to hosts, variation that translates directly to net costs to cheater wasps.

Who holds the reins? Context-dependent resource allocation in the mutualism between fig trees and their fig wasp pollinators

“…Decreased rates of abortions with increasing number of foundresses have previously been recorded in F. racemosa (Wang et al 2014) in China as we also found in our study. In a gynodioecious species Ficus hispida, although male trees showed decreased rates of g abortions with increasing foundress numbers, in female trees the effect was less pronounced especially under pollen-free foundress treatments (Zhang et al 2019). This indicates that sanctions differ between sexes, with male trees showing decreased sanctions against wasps since pollinator wasps develop only in syconia of male trees.…”

Egg load is a cue for offspring sex ratio adjustment in a fig‐pollinating wasp with male‐eggs‐first sex allocation

“…This trend could result from at least four not necessarily mutually independent processes. (a) Foundresses may lay eggs of ever‐reducing genetic viability (sensu Dunn et al, ), (b) of ever‐increasing susceptibility to host plant defences (sensu Dunn et al, ), (c) become depleted of the poison‐sac fluid for effective galling (Martinson et al, ) or (d) investment by trees to figs of variable pollen presence may cause increased larval mortality (Jander & Herre, ; Wang et al, ; Zhang et al, ). There is a lack of data in fig wasps on variation in larval viability, or susceptibility to plant defences, according to when eggs are laid during oviposition bouts, and whether or not gall failure is related directly to poison‐sac fluid reserves.…”

“…There is a lack of data in fig wasps on variation in larval viability, or susceptibility to plant defences, according to when eggs are laid during oviposition bouts, and whether or not gall failure is related directly to poison‐sac fluid reserves. However, a lack of pollen in several fig tree species, including F. racemosa , results in increased pollinator larval mortality (Jander & Herre, ; Jander, Herre, & Simms, ; Wang et al, ; Zhang et al, ). All figs involved in both of our experiments were pollinated but it was unavoidable that each fig received variable amounts of pollen.…”

“…Ovipositor‐excised wasps were introduced to ensure pollination, because focal wasps that had previously oviposited in their first fig would have become pollen‐depleted. The absence of pollen increases the likelihood of fig abortion or egg/larval mortality within un‐aborted figs (Wang et al, ; Zhang, Dunn, Wen, Sun, & Wang, ), which could thus be reduced by the introduction of pollen‐laden ovipositor‐excised foundresses.…”

“…This trend could result from at least four not necessarily mutually independent processes. sults in increased pollinator larval mortality (Jander & Herre, 2010;Jander, Herre, & Simms, 2012;Wang et al, 2014;Zhang et al, 2019). Wang et al, 2009).…”